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Published on March 9, 2007; 10.1104/pp.106.094979

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Received December 18, 2006
Accepted March 1, 2007

E2F Regulates FASCIATA1, a Chromatin Assembly Gene whose Loss Switches on the Endocycle and Activates Gene Expression by Changing the Epigenetic Status

Elena Ramirez-Parra and Crisanto Gutierrez *

Centro de Biología Molecular "Severo Ochoa", Consejo Superior de Investigaciones Científicas, Universidad Autónoma de Madrid, Cantoblanco 28049, Madrid, Spain

* Corresponding author; email: cgutierrez{at}cbm.uam.es.

Maintenance of genome integrity depends on histone chaperone-mediated chromatin reorganization. DNA replication-associated nucleosome deposition relies on the chromatin assembly factor 1 (CAF-1). Depletion of CAF-1 in human cells leads to cell death whereas in Arabidopsis, where it is involved in heterochromatin compaction and homologous recombination, plants are viable. The mechanism that makes the lack of CAF-1 activity compatible with development is not known. Here, we show that the FASCIATA1 (FAS1) gene, which encodes the CAF-1 large subunit, is a target of the E2F transcription factors. Mutational studies demonstrate that one of the two E2F binding sites in its promoters has an activator role while the other has a repressor function. Loss of FAS1 results in reduced CDKA activity, inhibits mitotic progression and promotes a precocious and systemic switch to the endocycle program. A selective up-regulation of the expression of a subset of genes, including those involved in activation of the G2 DNA damage checkpoint, also occurs upon FAS1 loss. This activation is not the result of a global change in chromatin structure but depends on selective epigenetic changes in histone acetylation and methylation within a small region in their promoters. This suggests that a correct chromatin assembly during S-phase is required to prevent unscheduled changes in the epigenetic marks of target genes. Interestingly, activation of the endocycle switch as well as introduction of activating histone marks in the same set of G2 checkpoint genes is detected upon treatment of wild type plants with DNA damaging treatments. Our results are consistent with a model in which defects in chromatin assembly during S-phase and the DNA damage signaling share part of a pathway, which ultimately lead to mitotic arrest and triggers the endocycle program. Together, this might be a bypass mechanism that makes development compatible with cell division arrest induced by DNA damage stress.




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